Malea et al. J of Biol Res-Thessaloniki (2018) 25:5 https://doi.org/10.1186/s40709-018-0076-4 Journal of Biological Research-Thessaloniki RESEARCH Open Access Cadmium uptake kinetics in parts of the seagrass Cymodocea nodosa at high exposure concentrations Paraskevi Malea1*, Theodoros Kevrekidis2, Konstantina‑Roxani Chatzipanagiotou1 and Athanasios Mogias2 Abstract Background: Seagrass species have been recommended as biomonitors of environmental condition and as tools for phytoremediation, due to their ability to concentrate anthropogenic chemicals. This study aims to provide novel information on metal accumulation in seagrasses under laboratory conditions to support their use as a tool in the evaluation and abatement of contamination in the feld. We investigated the kinetics of cadmium uptake into adult leaf blades, leaf sheaths, rhizomes and roots of Cymodocea nodosa in exposure concentrations within the range of 1 cadmium levels in industrial wastewater (0.5–40 mg L− ). Results: A Michaelis–Menten-type equation satisfactorily described cadmium accumulation kinetics in seagrass 1 parts, particularly at 0.5–5 or 10 mg L− . However, an S equation best described the uptake kinetics in rhizomes at 1 1 5 mg L− and roots at 10 and 20 mg L− . Equilibrium concentration and uptake rate tended to increase with the exposure concentration, indicating that seagrass displays a remarkable accumulation capacity of cadmium and refect high cadmium levels in the surrounding medium. Concerning leaf blades and rhizomes, the bioconcentration factor at equilibrium (range 73.3–404.3 and 14.3–86.3, respectively) was generally lower at higher exposure concentrations, indicating a gradual reduction of available binding sites. Leaf blades and roots accumulated more cadmium with higher rate than sheaths and rhizomes. Uptake kinetics in leaf blades displayed a better ft to the Michaelis–Menten- 1 type equation than those in the remaining plant parts, particularly at 0.5–10 mg L− . A marked variation in tissue 1 concentrations mainly after the steady state was observed at 20 and 40 mg L− , indicative of the stress induced on 1 seagrass cells. The maximum concentrations observed in seagrass parts at 5 and 10 mg L− were comparatively higher than those previously reported for other seagrasses incubated to similar exposure concentrations. Conclusions: Cymodocea nodosa displays a remarkable cadmium accumulation capacity and refects high cadmium levels in the surrounding medium. Kinetic models satisfactorily describe cadmium uptake in seagrass parts, primarily in adult leaf blades, at high exposure concentrations, permitting to predict cadmium accumulation in feld situations. Cymodocea nodosa appeared to be a valuable tool in the evaluation and abatement of cadmium contamination in coastal areas. Keywords: Metal, Accumulation kinetics, Seagrass parts, Cymodocea nodosa, Biomonitor, Phytoremediation Background productive ecosystems, provide habitat and nursery Seagrasses are present in most shallow coastal waters areas for a variety of invertebrates, fsh and mammals, throughout the world, providing a multitude of eco- and enhance water quality by stabilizing sediments and logical services and functions. Seagrass beds are highly removing nutrients [1]. Due to their ability to concentrate and retain non-nutrient anthropogenic chemicals in their tissues, seagrass species have been also recommended as *Correspondence: [email protected] 1 Department of Botany, School of Biology, Aristotle University biomonitors of environmental condition and as potent of Thessaloniki, 54124 Thessaloniki, Greece tools for phytoremediation [2–4]. Te usefulness of Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Malea et al. J of Biol Res-Thessaloniki (2018) 25:5 Page 2 of 11 seagrasses in the abatement of contamination in coastal considered as a species with great phenotypic plasticity areas is corroborated by available data suggesting that and a high capacity to adapt to environmental variability these plants appear to be relatively tolerant to many and thereby to colonize new substrates [22–24]. Cymodo- anthropogenic chemicals, particularly more tolerant than cea nodosa is also considered as a good biomonitor for other marine fora (macroalgae, kelp, saltmarsh plants, trace elements, with leaves being the best part for the mangroves) and macroinvertebrates [3]. determination of element loads [25]. In addition, micro- With regard to trace metals, which are of greatest envi- tubule integrity in leaf cells of C. nodosa is regarded as an ronmental concern [5], several studies, mainly in situ, early marker of metal-induced stress [18, 19, 26]. Under have examined the accumulation of these contaminants laboratory conditions, we investigated the kinetics of in seagrasses [3, 6]. Laboratory-derived results for metal cadmium uptake into adult leaf blades, leaf sheaths, rhi- uptake kinetics are available for about ten seagrass spe- zomes and roots of Cymodocea nodosa exposed to con- cies, for example Heterozostera tasmanica [7], Posi- centrations of cadmium ranging from 0.5 to 40 mg L−1; donia oceanica [8–10] and, most commonly, Zostera the uptake kinetics data were ftted to diferent models. species [11–13] and Halophila stipulacea [14–17]. Metal uptake kinetics only in one or two plant parts, namely Methods leaves or leaves and roots-rhizomes, were investigated Plant collection in most of these studies [7, 12–17]. Of the trace metals, Cymodocea nodosa was collected from the eastern coast cadmium, lead and zinc were more commonly used in of the Gulf of Tessaloniki, Northern Aegean Sea at uptake experiments [7, 9, 11–14, 16]. Recently, the link- the Viamyl site (site V, 40°33′N, 22°58′E). At this site, C. age between metal uptake into intermediate-juvenile leaf nodosa grows from 0.4 m to around 2 m depth, forming blades and toxic efects was also examined in a seagrass a continuous monospecifc meadow. Leaf, rhizome and species (Cymodocea nodosa) [18, 19]. However, only in root biomass displays an annual mean value of approx. a few of these studies, an attempt was made to describe 60, 122 and 65 g dry wt m−2, respectively [27]. Leaf bio- the uptake patterns by kinetic models [18, 19]. Te ft of mass and leaf blade length display an almost unimodal kinetics data to appropriate models would permit the cal- annual pattern; both markedly increase from March culation of uptake kinetic parameters and the prediction to July–August attaining a maximum value of approx. of metal accumulation in feld situations. Such informa- 150 g dry wt m−2 and 542.2 mm, respectively, while tion could support the use of seagrasses as a tool in the rhizome biomass and root biomass peak in mid or late evaluation of contamination in coastal areas or the clean- summer and in mid autumn to early winter attaining a up of contaminated sites. maximum value of approx. 225 and 125 g dry wt m−2, Te main goal of the present study is to contribute to respectively ([27], unpublished data). a better understanding of metal accumulation in sea- Plants were collected at the site V at 0.7–1.0 m depth grasses and to increase the utility of these marine plants in July 2011 with a 20 cm diameter acrylic corer, which as a potent tool in the evaluation and abatement of metal penetrated to a depth of 30 cm; all the above- and below- contamination in coastal areas. We assessed the capac- substrate plant material rooted within this area was col- ity of various parts of Cymodocea nodosa to accumulate lected. All plants were rinsed in seawater at the collection cadmium from the surrounding medium, as well as the site and transported to the laboratory in plastic contain- speed of this process. Cadmium was chosen as a con- ers containing seawater. taminant because it is considered highly toxic; it may enter the aquatic environment from various anthropo- Treatments genic sources, such as zinc, copper and lead mining, vari- Fresh green plants without epiphytes were kept for 24 h ous industries, nickel–cadmium batteries and phosphate in seawater under laboratory conditions in order to equil- fertilizers [20]. Cadmium concentrations in the range of ibrate. Plants were incubated in plastic aquaria contain- −1 0.1–100 mg L are typical in wastewater from several ing 10 L of cadmium sulphate hydrate (3CdSO 4·8H2O industries (chemical and metal product facilities, leather 98.7%, insoluble matter ≤ 0.005%, chloride ≤ 0.001%, and tanning processes, electricity and gas production total nitrogen ≤ 0.0005%, Ca ≤ 0.005%, Cu ≤ 0.0005%, and sanitary industries) [21]. Cymodocea nodosa (Ucria) Fe ≤ 0.0005%, K ≤ 0.01%, Na ≤ 0.005%, Pb ≤ 0.002%, Ascherson along with Posidonia oceanica (L.) Delile are Zn ≤ 0.002%; lot number: 1.02027.0100; Merck, Darm- the most important and widespread seagrass species stadt, Germany) dissolved in fltered (Whatman GF/C) in the Mediterranean Sea. Cymodocea nodosa is dis- seawater at one of the following cadmium concentrations: tributed from the intertidal zone to depths of 33–35 m, 0.5, 5, 10, 20 and 40 mg L−1, corresponding to 4.44, 44.48, and can colonize diferent environmental types, such as 88.95, 177.94 and 355.88 μΜ, respectively. Plant material open coastal waters, estuaries and coastal lagoons; it is of about 12.5 g dry wt, including about 70 leaf shoots and Malea et al. J of Biol Res-Thessaloniki (2018) 25:5 Page 3 of 11 the corresponding rhizomes and roots, was incubated in Data analysis each aquarium; no sediment and no complexing agents Cadmium accumulation kinetics were ftted to a ver- were added.